The Journal of Experimental Biology 207, 2777-2786 2777 Published by The Company of Biologists 2004 doi:10.1242/jeb.01092

Habitat-dependent transmission of male advertisement calls in bladder (; ) Vanessa C. K. Couldridge* and Moira J. van Staaden Department of Biological Sciences, and JP Scott Center for Neuroscience, Mind and Behavior, Bowling Green State University, Bowling Green, OH 43403, USA *Author for correspondence (e-mail: [email protected])

Accepted 18 May 2004

Summary It has been hypothesized that the physical properties of fynbos species had low levels of signal attenuation over the environment exert selection pressure on long-range distance in all environments. The fynbos biome was acoustic communication signals to match the local habitat characterized by high inconsistency in signal degradation, by promoting signal characteristics that minimize excess while the forest biome had the highest levels of attenuation and distortion. We tested this in a unique environmental noise. Innate habitat characteristics, family of bladder grasshoppers notable for producing a leading to comparatively limited acoustic communication signal with a 2·km maximum transmission distance. In distances in the forest and fynbos relative to the savanna direct performance comparisons, male advertisement calls and , may therefore explain the need for a of seven species were broadcast through four vegetation higher quality of signal transmission in grasshoppers biomes – forest, fynbos, savanna and succulent karoo. The inhabiting the former two environments. calls of species native to forest and fynbos biomes propagated with lower levels of distortion over distance in their respective habitats relative to those of non-native Key words: acoustic communication, advertisement call, habitat, species, while fynbos species also performed best in the bladder , Pneumoridae, sound transmission, remaining two habitats. In addition, both forest and spectrographic cross correlation.

Introduction Acoustic signals are commonly utilized for communication et al., 1986), and external properties of the local environment, over long distances by a variety of taxa, from butterflies incorporating vegetation type (Lang, 2000), meteorological (Yack et al., 2000) to elephants (McComb et al., 2003). conditions (Garstang et al., 1995), and acoustic interference However, one of the major predicaments plaguing long-range from other organisms (Wollerman, 1999). signallers is that sounds become progressively more degraded The acoustic adaptation hypothesis emanated largely from the further they propagate. The transmission of acoustic signals the work of Morton (1975) and Hansen (1979) and was through any given environment results in modification of the conceived as a means of means of investigating the relationship signal amplitude and fidelity over distance. Loss of amplitude, between animal vocalizations and ecological factors. This resulting from spherical spreading and also from absorption hypothesis was based on the observation that environmental and scattering of sound waves (excess attenuation), diminishes factors may heavily influence the evolution of long-range the range at which receivers can detect a signal, while loss acoustic signals by imposing selection pressures that act to of fidelity, incorporating frequency-dependent attenuation, modify the sound properties of signals in order to maximize irregular amplitude fluctuations and reverberations, reduces the their broadcast range and the number of potential receivers ability of receivers to accurately recognize a signal in the event (Endler, 1992; Forrest, 1994; Morton, 1975). This could lead it is detected. A combination of changes in both amplitude and to a matching between signal and environment, such that fidelity contributes to overall patterns of signal degradation. signals transmit optimally in native habitats and, conversely, The rate of acoustic signal degradation, and subsequently perform poorly when broadcast through non-native habitats. the range at which sounds can be used effectively for Studies concerning the propagation of long-range acoustic communication purposes, is dependent upon numerous factors. signals in relation to the environment in which they are These include spectral and temporal properties of the signal transmitted have yielded mixed results. The acoustic itself (Wiley and Richards, 1978), behavioural modifications adaptation hypothesis for enhanced transmission efficiency in of the animal during signalling, such as calling from native habitats has garnered support primarily from studies preferential heights and locations (Bennet-Clark, 1987; Keuper on avian and primate taxa. Birds inhabiting different 2778 V. C. K. Couldridge and M. J. van Staaden environments produce vocalizations with characteristics suited discernable differences in the female signal and the shorter to enhancing transmission in their native habitats (e.g. Bertelli transmission distances thereof. and Tubaro, 2002; Bowman, 1979; Cosens and Falls, 1984; Pneumorids are endemic to the coastal regions of southern Gish and Morton, 1981; Handford, 1981; Morton, 1975; Africa, where they are found in four distinct vegetation biomes: Wiley, 1991). Moreover, calls broadcast in different forest, savanna, fynbos (‘fine bush’) and succulent karoo environments exhibit differential rates of excess attenuation (Rutherford, 1997). These four habitat types represent a wide and/or distortion in both birds (e.g. Dabelsteen et al., 1993; Shy range of environmental conditions, varying in extremes from and Morton, 1986) and primates (e.g. Brown et al., 1995; dense, humid, forested areas to open, arid, semi-desert areas. Waser and Brown, 1986; Waser and Waser, 1977). In contrast, The forest biome is confined mostly to the wetter eastern the influence of the environment on the evolution of signal seaboard, where it is extremely patchy in distribution and characteristics has been more difficult to establish in anurans. comprises a very small total land area. Forest vegetation at the Most studies have failed to find a significant correlation site of transmission experiments comprised a closed canopy of between habitat acoustics and either signal characteristics woody vegetation up to 25·m tall and was dominated by (Zimmerman, 1983) or signal propagation (Castellano et al., Leucosidea sericea and Ficus thonningi, with trunk diameters 2003; Kime et al., 2000; Penna and Solís, 1998; but see Ryan reaching 1·m, and an understory of Maytenus acuminata, et al., 1990). Variability in detecting the effects of habitat Hypericum and Helichrysum spp. The subtropical savanna selection are likely to be due to the multiplicity of additional biome, by far the largest biome in , consists of factors that affect the evolution of signals. Mismatches grasses interspersed with taller woody vegetation. The area between signal and environment, which would potentially where experiments were conducted fell under the class of mask the effects of habitat selection, could arise from predator broad-leaved savanna. This is a typical C4 grassland with avoidance, competition avoidance, sexual selection, Themeda, Tristachya, Trachypogon and Aristida spp. being the phylogenetic history, and variation in the relative strengths of most prominent components, and average grass height reaching competing selection pressures. Here we test the acoustic approximately 0.5·m. The fynbos biome occupies the most adaptation hypothesis for bladder grasshoppers (Orthoptera, southern and south-western regions of southern Africa and is Pneumoridae) through an examination of acoustic signal characterized by evergreen, fine-leaved shrubs of intermediate transmission of species-specific male mating calls in different height. Fynbos vegetation is renowned for its unparalleled habitat types. This is the first detailed examination of the species diversity and is characterized by the presence of three relationship between the environment and sound propagation distinctive elements viz. restioids and ericoid shrubs, both in an invertebrate group specialized for long-distance ranging in height from 0.5·m to 2·m, and overstory proteoid signalling. We focus exclusively on habitat effects, since shrubs reaching a maximum height of 5·m (Cowling et al., constraints imposed by acoustic characteristics of the habitat 1997). The sparsely vegetated succulent karoo biome derives provide the framework within which other selection pressures its name from the low-lying leaf-succulent plants that dominate must operate. We thus anticipate an effect that is detectable, this biome. It is located along the western coast of southern though perhaps not strong. Africa and represents an intermediate state between the less arid Bladder grasshoppers comprise a small family of up to 17 fynbos to the south and true desert to the north. Succulent karoo species (Dirsh, 1965), with behaviour and morphology vegetation, although similar to fynbos in some respects, has a uniquely suited for pair-formation via acoustic duetting over relatively higher proportion of bulbous plants, and the distances of at least 50·m (van Staaden and Römer, 1997). With vegetation is lower growing, sparser, and comprises more the aid of an air-filled, inflated abdomen functioning as an succulents than fynbos. acoustic resonator, males produce a nocturnal advertisement Our primary objective was to evaluate the relative call that is both extremely loud (98·dB·SPL at 1·m) and importance of the environment in shaping signal evolution by relatively low in frequency (1.4–3.2·kHz) for an only comparing signal degradation across the four habitat types for 50·mm in length. Together with six pairs of highly sensitive seven species of bladder grasshopper. Of these, one species abdominal hearing organs (van Staaden and Römer, 1998), this (Pneumora inanis Fabricius) was classified as being native enables male signals to attain a viable transmission distance of to the forest, three (Bullacris intermedia Péringuey, B. up to 1.9·km at night (van Staaden and Römer, 1997). Male membracioides Walker, B. serrata Thunberg) native to the signalling functions as the primary basis for pair formation, savanna, two (B. obliqua Thunberg, Physemacris variolosus with non-flighted receptive females producing a softer L.) native to the fynbos, and one (B. unicolor L.) native to the response, enabling flighted males to locate them. The male succulent karoo. With one exception, all species have advertisement calls of pneumorids possess a high degree of geographic ranges that fall exclusively into one biome. species specificity, displaying substantial variation in both However, B. unicolor, which is predominantly a succulent temporal and structural properties among species. However, karoo species, extends slightly into the fynbos along the edges despite these broad interspecific differences in the male signal, of its geographic distribution. In concordance with the acoustic courtship and mating follow a stereotyped sequence in all adaptation hypothesis, we test the prediction that the species, and female calls are virtually indistinguishable. Here transmission efficiency of long-distance signals is greater in we focus our attention on male signals, due to both the lack of native habitats relative to that in non-native habitats, Bladder grasshopper signal transmission 2779 specifically with respect to (i) transmission distance and (ii) signal fidelity.

Materials and methods Field sites Field experiments were conducted between 20:00·h and 24:00·h during January and October 2002, coinciding with both the active time-period and the seasonal occurrence of the . Four locations in South Africa with undisturbed vegetation, each falling within one of the biomes of interest, were selected as field sites for the transmission experiments (Fig.·1). These were: (1) Goegap Nature Reserve in Springbok, Northern Cape province: succulent karoo biome; (2) Wolfkop Private Nature Reserve in Citrusdal, Western Cape province: Fig.·1. Map of South Africa showing the four biomes of interest and fynbos biome; (3) Krantzkloof Nature Reserve in Kloof, the locations of the field sites where the transmission experiments KwaZulu-Natal province: savanna biome; and (4) a private were conducted: 1, Springbok; 2, Citrusdal; 3, Kloof; 4, Bulwer. Lines farm at Bulwer, KwaZulu-Natal province: forest biome. Mean within South Africa indicate provincial boundaries. relative humidity and temperature measures for the field sites were estimated at 58% and 18°C in the succulent karoo, 63% and 16°C in the fynbos, 87% and 21°C in the savanna and 69% pauses of 3·s for repetitions of the same call and 5·s for and 19°C in the forest. different calls minimized the risk of forward-masking. In other words, this time window was sufficient to prevent Test sounds reverberations of the previous call overlapping with the next Sound recordings of male advertisement calls used in the signal. transmission experiments (i.e. test sounds) were exemplars selected from a previously recorded sound library. These songs Transmission experiments were recorded in the laboratory using a sound level meter Experiments were carried out in which advertisement (Bruel & Kjaer, model 2009; Naerum, Denmark) and a signals of seven pneumorid species were broadcast and re- microphone (1/2” condenser, type 2540, Larson & Davis, recorded along a transect at various distances and heights from Provo, UT, USA; A weighting, RMS fast) placed 1·m dorsal the sound source. An identical protocol was followed in each to a calling male in a wire mesh cage. Songs were sampled at of four habitat biomes. All sound transmission experiments 44.1·kHz on an Apple Macintosh Powerbook via the built- were conducted when wind speed was less than 1·m·s–1 and in 16-bit A/D soundboard and subsequently edited with ambient noise levels relatively low. A single speaker elevation SoundEdit™16 (San Francisco, CA, USA). Male call (1.5·m) and three microphone heights (0.2·m, 1·m, 2·m) were characteristics, including length, frequency and temporal selected as representative caller heights and receiver locations, patterning, vary substantially among species (Table·1, Fig.·2). respectively. Signal propagation was assessed for three Background noise was generally low in the laboratory setting, different receiver elevations, since female restriction to their thus test sounds had equivalent low levels of background noise specific host plants determines the most likely transmission for each species. For each species, a single exemplar was channel. Males of most bladder grasshopper species call at the selected, based on average call characteristics for the species. intermediate height of 1.5·m (M. J. van Staaden, personal For ease of comparison, all calls were amplified to a uniform observation), corresponding with the maximum vegetation peak amplitude value (amplification range: 0.8–19.1·dB). The height in most habitats. The only notable exception is the order of signal presentation was randomized and inter-song forest-dwelling P. inanis, which has a propensity to call at

Table·1. Physical characteristics of the male bladder grasshopper advertisement calls used in the study Final Peak frequency Call length syllable length Number of Final Species (kHz) (s) (s) short syllables syllable repeated B. intermedia (Savanna) 1.81 2.87 1.10 6 No B. membracioides (Savanna) 1.72 2.55 0.77 5 No B. serrata (Savanna) 2.15 1.44 1.13 2 No B. unicolor (Succulent karoo) 2.07 2.34 1.12 2 No B. obliqua (Fynbos) 1.55 5.83 4.16 4 No Ph. variolosus (Fynbos) 3.19 0.66 0.30 2 No Pn. inanis (Forest) 1.46 9.93 0.28 6 Yes, 10× 2780 V. C. K. Couldridge and M. J. van Staaden higher elevations. Test sounds were broadcast from an Apple positioned microphone was shock mounted (Audio-Technica G4 laptop computer running SoundEdit™16, and passed AT 8415, Tokyo, Japan) on a 2·m extendible rod, and aligned through a Pioneer GM-X252 amplifier connected to a Jensen with the loudspeaker by eye. Recordings at a distance of 1·m 6944 loudspeaker at the origin of the transect. The broadcast were taken at a height of 1.5·m only, level with the speaker. signal was adjusted to a maximum intensity level of 95·dB·SPL Under these circumstances, the sounds had suffered negligible (re 20·µPa) at a distance of 1·m, as measured with a Larson- habitat-induced degradation, and served both as a control for Davis DSP83 sound level meter. This value was selected based any sound distortion caused by the recording system and as on the known value for B. membracioides, the only species for calibration signals with which to compare recordings taken at which natural sound intensity levels have been reliably greater distances. Six repetitions of each call were recorded at recorded. While the values for B. membracioides are believed each distance and height over two consecutive nights, in order to be similar to the natural calling intensity levels of the other to better represent the natural variability present under field species, the possibility exists that some species may call at conditions. intensities either higher or lower than the chosen broadcast intensity. Within B. membracioides, males always call at the Data analysis maximal recorded intensity level to advertise their presence, All control (recorded at a distance of 1·m) and observation and only reduce the amplitude of their calls when in close (recorded at distances greater than 1·m) sounds were digitized proximity to a responding female. onto an Apple MacIntosh G4 computer via the built-in sound- In each of the four field sites, a 100·m straight line transect board (44.1·kHz sampling rate; 16·bit sample size) and filtered was marked out along a flat stretch of land bearing with Canary 1.2 (Canary: the Cornell Bioacoustics representative vegetation. This distance corresponds to the Workstation, Version 1.2. Cornell Laboratory of Ornithology, maximum transmission distance at the behavioural response Ithaca, NY, USA; 1995) to remove frequencies below 500·Hz threshold of female B. membracioides (van Staaden and and above 12·kHz. This filtering did not compromise any Römer, 1997, 1998). The broadcast sounds were re-recorded components of the test signal itself. Through auditory and along the transect at six distances (1·m, 5·m, 10·m, 25·m, 50·m, sonogram inspection, we selected as a control sound one of the 100·m) from the sound source using a Marantz PMD 430 three repetitions of each test signal recorded at 1·m that was (Setagaya, Japan) audio cassette recorder connected via a not superimposed by transient noise fluctuations. Data analysis 6·m cable to a wind-shielded, unidirectional microphone involved comparisons between filtered, degraded observation (Sennheiser MZW 66; Wedemark, Germany). The horizontally sounds, and their respective species-specific, undegraded control sounds. Quality of signal transmission was assessed via two measurements. Overall signal amplitude was used as a measure of attenuation over distance and spectrographic cross correlation (described below) served as a measure of distortion over distance. Spectrograms were created for each of the signals using a transform length of 256 points and cross correlation Pn. inanis analysis performed on these. Control and observation (Forest) signals were aligned at the start, the two signals slid past each other, and a correlation coefficient calculated for each 6 point in time based on both temporal and amplitude differences between the two calls. The maximum cross 4 correlation coefficient obtained from each comparison was Hz k 2 plotted against recording distance for each species in each 0 habitat type and height. A curve was then fitted to each of 1 s B. intermedia B. membracioides B. serrata these 84 plots and the values of the slopes of the curves (Savanna) (Savanna) (Savanna) used in subsequent analyses. Because data were normally distributed, three-way analysis of variance (ANOVA) was used to test for differences in signal transmission, with broadcast habitat, native habitat and recording height as independent variables. Signal attenuation was analyzed by measuring the average intensity for each signal and then plotting this Ph. variolosus B. obliqua B. unicolor value against recording distance in a similar manner to that (Fynbos) (Fynbos) (Succulent karoo) described above. The slopes of the curves were again used Fig.·2. Sonogram exemplars of species-specific male mate location to evaluate differences in signal transmission. signals for seven bladder grasshopper taxa used in the transmission In addition, ANOVAs were used to analyze both cross experiments. correlation coefficients and amplitude at the maximum Bladder grasshopper signal transmission 2781 recording distance of 100·m, to assess differences among Comparisons of cross correlation coefficients at a distance species within each vegetation biome. Due to the logarithmic of 100·m revealed that the native forest species performed nature of the dB scale, amplitude values in dB were converted significantly better than all other species in the forest habitat into sound pressure values for the analysis and then converted at heights of both 1·m and 2·m, and significantly better than all back into dB. except the succulent karoo species at a height of 0.2·m Standard deviations (S.D.) of both cross correlation and (Fig.·3A). In the fynbos (Fig.·3B), inhabitant species had intensity data were used to assess consistency of signal significantly higher correlation coefficients than all other transmission. No significant differences in consistency (S.D.) species at recording heights of 1·m and 2·m, although there were detected among any species for either cross correlation were no significant differences at a height of 0.2·m. In their or intensity, and data from all species were therefore pooled to native habitat, savanna species outperformed the succulent examine differences among habitats, using ANOVAs. karoo species at 0.2·m and 1·m heights, but fared significantly Environmental noise was estimated separately in each worse than fynbos species at 0.2·m and 2·m heights (Fig.·3C). habitat by compiling 10·s of uncorrupted background noise Finally, in the succulent karoo, the indigenous species had from the silence between consecutive test sounds. From these, significantly lower correlation coefficients than fynbos species power spectra were derived representing background noise at 0.2·m and 2·m, and than fynbos and savanna species at 1·m along the entire transect throughout the experimental session. (Fig.·3D).

Attenuation of transmitted grasshopper calls Results The habitat in which signals were broadcast, the native A total of 3024 recorded signals were digitized for analysis, habitat of the grasshoppers, and the height at which signals of which 204 (6.7%) were excluded from the data set due to were recorded all had a strongly significant effect on the transient noise fluctuations. Consequently, there were amplitude of transmitted signals (Table·3). Height also had a sometimes less than the maximum of six repetitions of each significant interaction with broadcast habitat, indicating that signal at each distance and height combination. calls attenuate differently in different habitats at similar heights. Distortion of transmitted grasshopper calls Comparisons of amplitude measures at a maximum There was a significant interaction between native habitat recording distance of 100·m are shown in Fig.·4. The call of (the resident habitat of the pneumorid producing the call) and the forest species attenuated significantly less in its native broadcast habitat (the habitat in which the call was broadcast) habitat than all other species at a height of 0.2·m, less than in the three-way ANOVA of spectrographic cross correlation, savanna and succulent karoo species at a height of 2·m, and indicating that calls distort differently when broadcast in native less than savanna and succulent karoo species, but more than versus non-native habitats (Table·2). In addition, there were fynbos species, at a height of 1·m (Fig.·4A). Fynbos species marginally non-significant differences in broadcast habitat, had significantly higher amplitudes in the fynbos habitat than recording height and the interaction between these two factors savanna and succulent karoo species at each of the three (Table·2). This suggests that call distortion varies heights (Fig.·4B). Native species in the savanna had independently according to both the habitat through which it significantly lower amplitudes than forest and fynbos species is being transmitted and the height at which it is being at all three heights and significantly higher amplitudes than the transmitted, and that calls may transmit differently at given succulent karoo species at 0.2·m and 1·m heights only heights in different habitats. (Fig.·4C). In the succulent karoo, the inhabitant species had

Table·2. ANOVA on regression slopes of cross correlation Table·3. ANOVA on regression slopes of signal amplitude coefficients over distance over distance Source d.f. Sum of squares F-ratio P Source d.f. Sum of squares F-ratio P Model 47 0.02648266 4.082 <0.001* Model 47 341.68601 9.235 <0.001* Broadcast Habitat 3 0.00174112 2.773 0.051 Broadcast Habitat 3 68.47082 28.991 <0.001* Native Habitat 3 0.00106951 1.704 0.178 Native Habitat 3 51.13323 21.650 <0.001* Height 2 0.00083037 3.968 0.052 Height 2 99.92324 63.463 <0.001* Broadcast × Native 9 0.00601000 3.191 0.004* Broadcast × Native 9 8.49397 1.199 0.326 Broadcast × Height 6 0.00165911 2.643 0.059 Broadcast × Height 6 36.83090 7.797 <0.001* Native × Height 6 0.00009435 0.150 0.929 Native × Height 6 5.53834 1.173 0.343 Broadcast × Native 18 0.00077820 0.413 0.922 Broadcast × Native 18 15.14157 1.069 0.418 × Height × Height Error 36 0.01088200 Error 36 28.34117 Total 83 0.03736466 Total 83 370.02718

*Significant, P<0.05. *Significant, P<0.05. 2782 V. C. K. Couldridge and M. J. van Staaden

A Forest Fig.·3. Cross correlation coefficients 0.55 (means ± S.E.M.) at a recording distance of 100·m in four transmission 0.50 habitats and at three recording heights. a a Species are grouped according to their a 0.45 native habitats. Letters above error a b b bars (a–c) indicate significance bc 0.40 b individually within each plot, with b different letters representing a c c 0.35 b significant difference at the 5% level and the same letter indicating no 0.30 significant difference.

Fynbos 0.55 B among habitats (F3,417=38.351; P<0.001; Tukey multiple 0.50 a a a comparison tests), with least a a b a b b b b variable distortion in forest and 0.45 b succulent karoo habitats, followed 0.40 by the savanna and then by the

t fynbos (Fig.·5). Variation in sound n e 0.35 distortion increased with distance

ffici from the speaker and as height oe

c above ground decreased.

0.30 n

o Consistency of signal attenuation i t a

l also varied significantly among 0.55 C Savanna habitats (F =63.133; P<0.001;

orre 3,417 c a a Tukey multiple comparison tests), 0.50 ab ross a bc b b with the highest consistency C b c b 0.45 bc exhibited in the forest and the c lowest in the fynbos (Fig.·6). 0.40 Savanna and succulent karoo habitats were intermediate 0.35 between these two and did not differ from each other. As 0.30 expected, variation in attenuation was extremely low in the forest, 0.55 D Succulent karoo and changed with neither recording distance nor height. In the other 0.50 three habitats, consistency increased noticeably with distance a at elevations of 1·m and 2·m. 0.45 a a b b However, at 0.2·m recording ab b b b 0.40 bc c height there was little or no b relationship between standard 0.35 deviation and distance.

0.30 Environmental noise For Fyn Sav Suc For Fyn Sav Suc For Fyn Sav Suc Levels of ambient background Native habitat (0.2 m) Native habitat (1 m) Native habitat (2 m) noise varied appreciably among localities (Fig.·7). Background significantly greater attenuation than forest and fynbos species noise in the forest was higher than in any other habitat and at a height of 2·m, but showed no significant differences at both consisted mainly of the sounds of water running in nearby 0.2·m and 1·m heights (Fig.·4D). streams and of calling frogs. The savanna was also relatively noisy and was predominated by the songs of crickets and Consistency of grasshopper calls other . Both the fynbos and the succulent karoo Consistency of signal distortion differed significantly appeared to have less background noise than the other two Bladder grasshopper signal transmission 2783

Fig.·4. Amplitude measurements (means ± 60 A Forest S.E.M.) at a recording distance of 100·m in four transmission habitats and at three 55 a a a recording heights. At this distance, b c b attenuation due to spherical spreading alone 50 c b theoretically results in an amplitude of a 56.4·dB. Species are grouped according to b 45 their native habitats. Letters above error c c bars (a–c) indicate significance individually 40 within each plot, with different letters representing a significant difference at the 35 5% level and the same letter indicating no significant difference. 60 B Fynbos

55 Discussion Our results demonstrate that male a ab a 50 bladder grasshopper advertisement a a ab b b calls transmit more favourably in 45 b b native as opposed to non-native b b habitats, at least in some species. In 40 accordance with the predictions of the acoustic adaptation hypothesis

(dB) 35 (Morton, 1975), native signals out- e d performed non-native signals in forest tu 60 C Savanna and fynbos habitats, but this finding did not hold for the savanna and succulent Ampli 55 ab a a a karoo habitats. Fynbos species b performed consistently well in all c b b 50 a a environments except the forest in terms b of signal distortion, whereas either 45 forest or fynbos species predominated c in most instances in terms of signal 40 attenuation. The pattern of performance of 35 species’ signals in the forest was distinctly different to that in the other 60 D Succulent karoo three habitats, which all produced similar results. Although transmission 55 in the savanna, fynbos and succulent a karoo habitats yielded different levels 50 of signal degradation, the relative a b ab ab a bc ab relationship among species remained 45 b comparable. This may be explained in b ab c part by structural differences in the 40 type of vegetation among the four habitats. Whereas the forest represents 35 a closed habitat dominated by 5–25·m For Fyn Sav Suc For Fyn Sav Suc For Fyn Sav Suc high trees and several understory Native habitat (0.2 m) Native habitat (1 m) Native habitat (2 m) layers, the other habitats are all more open with predominately low-lying vegetation (<1·m), sparsely habitats. The fynbos was mostly characterized by a few interspersed with taller (1–2·m) shrubs. Moreover, while calling frogs and night birds, and the succulent karoo by the structural features are likely to be of greater import than calls of insects. In addition, background noise in the forest floristic ones, it is notable that fynbos and succulent karoo was continuous, whereas in the other habitats it was biomes share 55% of their species diversity (Rutherford, 1997). intermittent. It is therefore not surprising that at this level, our observations 2784 V. C. K. Couldridge and M. J. van Staaden

0.07 0.07 conform to expectations, with species Forest Fynbos performing similarly in the savanna, 0.06 0.06 0.2 m fynbos and succulent karoo, 0.05 1 m 0.05 particularly at higher elevations, and 2 m 0.04 0.04 performance in the forest differing significantly from that of the open 0.03 0.03 habitats. . D . Recent studies have stressed the

S 0.02 0.02 importance of broadcast variability as 0.01 0.01 a critical consideration in the evolution 0 0 of signals, perhaps even more so 0 20406080100 0 20406080100 than broadcast quality (Brown and Handford, 2000, 2003). Although we 0.07 0.07 Savanna Succulent karoo found no differences in transmission 0.06 0.06 variation among species, we did identify substantial differences 0.05 0.05

Cross correlation coefficient among habitats. Interestingly, signal 0.04 0.04 degradation in the fynbos was far more variable than in any other habitat and 0.03 0.03 may provide an explanation as to why 0.02 0.02 the calls of the native fynbos species 0.01 0.01 performed admirably in all habitats. Selection pressure to maximize the 0 0 reliability of information transfer in the 0 20406080100 0 20 40 60 80 100 signals of fynbos species potentially Distance (m) Distance (m) derives from two sources, viz. inherent Fig.·5. Standard deviations of cross correlation coefficients plotted over distance at three characteristics of the transmission different heights above the ground in four different habitats. channel and inter-specific acoustic competition. The acoustic signals of 5 5 Forest Fynbos native fynbos species are characterized by either relatively low-frequency 4 4 0.2 m calls, or very brief, high-frequency 1 m calls (Fig.·2), design features that 3 2 m 3 could compensate for the lack of transmission reliability in their native 2 2 habitat. In addition, pneumorid species 1 1 diversity and sympatry achieve their

. highest levels in the fynbos habitat. D . S 0 0 The two fynbos species considered 0 20406080100 0 20406080100 here are sympatric in at least part of their range, as well as with other 5 5 pneumorid species not considered here

Amplitude Savanna Succulent karoo (Dirsh, 1965). This temporal and 4 4 spatial overlap means that males of several species may frequently call 3 3 together in the same area, placing further selection pressure on the 2 2 transmission channel to produce calls that can be clearly distinguished from 1 1 those of heterospecifics. In light of this distribution overlap, fynbos species 0 0 may have increased the transmission 0 20406080100 0 20406080100 quality, rather than the consistency of Distance (m) Distance (m) their signals, and these features cannot Fig.·6. Standard deviations of amplitude measurements (mean ± S.D.) plotted over distance at simultaneously be maximized in open three different heights above the ground in four different habitats. habitats (Brown and Handford, 2000). Bladder grasshopper signal transmission 2785

0 on call transmission, particularly in P. variolosus, which has Forest Fynbos an exceptionally short advertisement call. Reducing the –15 duration of high frequency signals appears to be an effective –30 adaptive mechanism to counteract degradation, irrespective of habitat type. –45 Ambient environmental noise is a form of acoustic –60 interference that can mask signals in the same frequency range, and noise levels have previously been implicated in song 0 divergence among populations within a species (Slabbekoorn Savanna Succulent karoo –15 and Smith, 2002). It is possible that environmental noise is Power (relative dB) placing selection pressure on bladder grasshoppers to avoid –30 calling in the same frequency range as either other animals or –45 abiotic factors in their local environment. Indeed, virtually all species tested here produced calls with peak frequencies –60 0 5 10 15 20 0 5 10 15 20 mismatched to the dominant frequencies of ambient noise, Frequency (kHz) from both biotic and abiotic sources, in their native habitats. The only exception was B. unicolor in the succulent karoo, Fig.·7. Power spectra of environmental noise in the four different which calls at a peak frequency that corresponds closely habitats where transmission experiments were performed. The dotted (within 200·Hz) with the most dominant frequency of lines represent the carrier frequencies of the signals of species native background noise in its indigenous habitat. The precise source to that habitat. of this intermittent call is, as yet, unidentified, but the acoustic challenge the species presents for B. unicolor may constitute Height above ground level is an essential consideration in a telling exception to the apparent facility of bladder the transmission of sounds (Dabelsteen et al., 1993; Marten and grasshoppers for maintaining a private communication Marler, 1977; Mathevon et al., 1996; Waser and Waser, 1977). channel. We found cross correlation coefficients to be similar at all three Only thirteen species of bladder grasshopper have males heights, indicating that, in contrast to the situation with birds displaying the primary morph of an inflated abdomen (Dirsh, (Holland et al., 1998), elevation did not play a large role in 1965) and thus have the potential to produce long-distance signal distortion. Elevation did, however, have considerable mating signals. The seven species included in this study were impact on signal attenuation, which was much more those for which quality sound recordings are available, and pronounced closer to the ground. Consistency in signal represented the four vegetation types in unequal numbers of propagation was also found to vary in accordance with height. between one and three species per biome. This inequality and Degradation was more variable at lower elevations and the lack of multiple representations of native species in two variation increased with distance at all three heights. Variation habitats are unfortunate, but unavoidable. Pneumorids are in attenuation tended to remain static at 0.2·m, but increased notoriously difficult to find in the field and the calls of six with distance at higher elevations. It should be noted that in species have not yet been recorded. While a comprehensive our experimental design, the speaker was always kept at a picture of the effects of habitat acoustics on the evolution of constant height above the ground and only the position of the male advertisement signals in this particular taxon would microphone was varied. It is likely that elevation would have indubitably benefit by including some of the currently more had a much more pronounced effect had the broadcast height elusive species, the present study demonstrates that signal been adjusted in accordance with the receiver height. structure varies among species in ways that reflect acoustically The frequency dependency of the pattern of excess relevant differences in the environment. Different attenuation accumulation with transmission distance has been environments favour qualitatively different traits, thus widely documented (Lang, 2000; Marten and Marler, 1977; supporting long-term evolutionary effects of habitat acoustics Morton, 1975; Naguib, 1995). However, we found no on signals and signalling behaviour (sensory drive; Endler, significant correlation between call frequency and transmission 1993). in bladder grasshoppers. This lack of correlation was mostly The results presented here provide support in an invertebrate due to the anomaly of P. variolosus emitting a comparatively group for the acoustic adaptation hypothesis of covariance of high frequency signal, yet being one of the species with the acoustic signals and habitat characteristics in a manner that highest transmission performances. Indeed, if P. variolosus is maximizes communication range. Moreover, they provide a removed from the analysis, the relationship between call bridge between the evolutionary history of the group and the frequency and degradation becomes significant in the predicted ecological drive on the sensory system. A striking feature of direction. Furthermore, carrier frequency and call length are the results is that while environmental selection explains some strongly negatively correlated in the species under examination of the observed signal diversity of bladder grasshoppers, the here (Spearman Rho=–0.9643; P<0.001) and this relationship effects of selection on species-specific advertisement calls are with call length may well be masking the effect of frequency rather uneven. This discrepancy may be attributable in part to 2786 V. C. K. Couldridge and M. J. van Staaden variation in selection pressure; those species inhabiting Handford, P. (1981). Vegetational correlates of variation in the song of environments less conducive to sound propagation over Zonotrichia capensis. Behav. Ecol. Sociobiol. 8, 203-206. Hansen, P. (1979). Vocal learning: its role in adapting sound structures to extended distances likely face stronger selection pressures long-distance propagation, and a hypothesis on its evolution. Anim. Behav. to modify their signal characteristics in accordance with 27, 1270-1271. environmental properties. Furthermore, additional factors Holland, J., Dabelsteen, T. and Pedersen, S. B. (1998). Degradation of wren Troglodytes troglodytes song: implications for information transfer and not considered here, such as female choice, male–male ranging. J. Acoust. Soc. Am. 103, 2154-2166. competition, density and variety of predators, and phylogenetic Keuper, A., Kalmring, K., Schatral, A., Latimer, W. and Kaiser, W. constraints, may all have had far-reaching impacts on signal (1986). Behavioural adaptations of ground living bushcrickets to the properties of sound propagation in low grassland. Oecologia 70, 414-422. evolution. The simultaneous coupling of these factors with Kime, N. M., Turner, W. R. and Ryan, M. J. (2000). The transmission of environmental factors may account for the complex observed advertisement calls in Central American frogs. Behav. 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